The offer is part of a new theatre scheme called Writers’ Block, which aims to address the cost of London accommodation for playwrights from underprivileged backgrounds.
Waller-Bridge, who is also an actor and writer, has donated the flat for use by emerging writers and made what has been described as a “generous financial contribution” to the scheme.
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Writers will live in the flat rent-free and only be asked to cover the cost of bills during their stay.
The scheme is backed by a number of leading figures from the theatre and film industries, including Jack Thorne, co-creator of Adolescence and writer of Harry Potter and the Cursed Child, and Waller-Bridge’s partner Martin McDonagh, who is best known for writing and directing films including Oscar and Bafta-winning The Banshees Of Inisherin and Three Billboards Outside Ebbing, Missouri.
Mr Thorne said: “I was lucky when I started out, my brother lived in Croydon and was able to put me up.
“He did so, rather selflessly, for five years, before I moved to Luton and he got his peace.
“For many writers the need for a roof makes writing impossible, which is why this pilot is so important.
“If you’re from privilege your biggest problem is what to fill a page with, if you’re not, so much of your struggle is about the need to survive.”
The project has also received support from playwright and screenwriter James Graham, Happy Valley creator Sally Wainwright, and The Crown’s Peter Morgan.
Mr Graham said: “The industry’s urgent pursuit of representation is still letting down the biggest area of under-representation of all, which is class.
“When I first made it to London, I slept on friend’s floors and worked in call centres and bars while I wrote.
“Every spare room a scheme like this can give to writers starting out in London, not only helps them write but saves them from giving up completely.
“We don’t need grand gestures, just someone to open a door and help us keep going.”
Writers’ Block is an evolution of the Adopt a Playwright Award, launched in 2008 to support writers from disadvantaged backgrounds by offering affordable accommodation in London for meetings, rehearsals, performances and career opportunities.
Both schemes were created by Sofie Mason and Diana Jervis-Read, founders of The Offies, the Off West End Theatre Awards.
Ms Mason and Ms Jervis-Read have highlighted research from the Creative Industries Policy and Evidence Centre and the Sutton Trust showing that only 16 per cent of people working in the creative industries come from working-class backgrounds.
So far, 55 writers have received support through the Adopt a Playwright scheme.
Writers’ Block is delivered in partnership with Omnibus Theatre in Clapham and connects playwrights with hosts who have a spare room or property and are willing to offer it at dramatically reduced rates.
Irish actor Alan Turkington, known for his role in the Netflix series Heartstopper, has taken part in the scheme by offering a room in his Camberwell flat.
Mr Turkington said: “I’m so happy that I became an early adopter of this scheme and I’m even happier to champion it.
“I was very lucky to afford a flat in the late 90s and have tried to pay some of that privilege forward, especially now when rents are abhorrently high.
“I have rented out my spare room for years, largely to creatives, and have come to realise that writers in particular have such a strong work ethic, with a huge respect for both their space, mine and our shared home.
“To me, being an Omnihost is the most decent and worthwhile way to rent out a room if you have one.”
Mr McDonagh, who is also supporting the scheme, is best known for writing and directing films including Oscar and Bafta-winning The Banshees Of Inisherin and Three Billboards Outside Ebbing, Missouri.